disease management strategies for wildlifedisease management strategies for wildlife summary three...

IntroductionThe desire or need to actively manage infectious disease in wildanimals is a relatively recent phenomenon, compared to healthmanagement in humans and domestic animals. In the past,occurrence of infectious disease among wild animals receivedlittle attention except when major events occurred, ofteninvolving the health of humans or domestic animals.Management of disease in wild animals is usually undertakenfor some reason that will benefit humans, such as reducing or

controlling zoonotic diseases, diseases shared with domesticanimals, or disease conditions considered to be detrimental tospecies valued by humans. Interest in diseases of wild specieshas increased recently for several reasons including:

– emergence of zoonoses, such as Lyme disease, varioushaemorrhagic fevers and hantavirus pulmonary syndrome, thathave been traced to wild animals

– recognition that wild animals are a reservoir for diseases, suchas bovine tuberculosis and brucellosis, that may prevent theelimination of these diseases from domestic animals

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Disease management strategies for wildlife

SummaryThree basic forms of management strategies exist for wildlife disease, as follows:prevention of introduction of disease, control of existing disease or eradication.Management may be directed at the disease agent, host population, habitat or befocused on human activities. Disease agents may be dealt with in theenvironment through disinfection or in the host through treatment. Disinfectionand pesticides used to destroy agents or vectors are limited to local situations,may have serious environmental effects and may result in acquired resistance.Difficulty in delivering treatment limits chemotherapy to local situations. Hostpopulations may be managed by immunisation, by altering their distribution ordensity, or by extirpation. Immunisation is best suited for microparasiticexogenous infections with a low reproductive rate and in populations which havea low turnover. Mass immunisation with oral baits has been effective, but thisstrategy is limited to a few serious diseases. It is difficult to move wild animalsand techniques to discourage animals from entering an area become ineffectiverapidly. The setting up of fences is feasible only in local situations. Selectiveculling is limited to situations in which affected individuals are readily identifiable.General population reduction has had little success in disease control butreducing populations surrounding a focus or creating a barrier to diseasemovement have been successful. Population reduction is a temporary measure.Eradication of a wildlife population has not been attempted for diseasemanagement. Habitat modification may be used to reduce exposure to diseaseagents, or to alter host distribution or density. Management of diseases of wildanimals usually requires a change in human activities. The most importantmethod is by restricting translocation of wild animals to prevent movement ofdisease.

Keywords Control – Eradication – Microparasites – Macroparasites – Management – Prevention –Transmission – Vectors – Wildlife.

G. Wobeser

Department of Veterinary Pathology, Western College of Veterinary Medicine, University of Saskatchewan,52 Campus Drive, Saskatoon, Saskatchewan S7N 5B4, Canada

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– increased domestication of indigenous species, such as elk(Cervus elaphus) and deer (Odocoileus spp.), for game farmingwith the attendant risk of disease transmission to and from free-ranging animals

– increased awareness of risks inherent in the translocation ofwild species together with their infectious diseases

– general concern about the well-being of wild populationsaffected by habitat degradation, fragmentation and loss

– emergence of conservation biology with intensivemanagement of threatened or endangered species.

Concurrently, there has been a marked increase in interest inthe study of population and evolutionary aspects of parasitesand host-parasite relationships by ecologists. Most of suchinvestigations have not been concerned directly with diseasemanagement, but they have provided a theoretical basis fordisease management.

Infectious disease, induced by parasitic organisms, is a normalfeature of the life of wild animals and the typical wild animalhosts a broad multi-species community of potentially harmfulparasitic organisms. This is quite different from the situation inmany human and domestic animal populations. In developedcountries, infectious disease now plays a minor role in humanhealth and the expectation is that most people will survive wellbeyond the age of reproduction to old age. Infectious disease ismore common in intensively managed livestock than inhumans but the expectation is that the great majority ofdomestic animals will survive and thrive until they havefulfilled their intended purpose. Thus, the farmer plansreproduction in animals to produce approximately the numberneeded to fit the market. In contrast, among wild animals,reproduction is far greater than necessary to maintain thepopulation if most animals were to survive to old age. Mostindividuals of most species die at a young age, often beforereaching sexual maturity. This high rate of mortality is causedby a variety of factors including predation, malnutrition,accidents and disease, which are interrelated and seldom actindependently.

Disease management –important conceptsTwo questions should be addressed early in the discussion ofmanagement of disease in wild species. The first is thedesirability of altering the course of disease in free-livinganimals. Parasitism is a powerful ecological and evolutionaryforce in the natural biology of all species. For this reason, onecould argue that any intervention to alter the course ofinfectious disease in wild animals is an undesirable intrusion.However, there is also accumulating evidence that the dynamicrelationship between disease agents and host species can bedisrupted severely by changes in their shared environment.

Most of such environmental disruptions result from humanactivity and no wild animal lives in an environment that has notbeen modified in some manner by humans. For this reason,disease management can be viewed as an attempt to mitigateother human actions. Some authors feel strongly that this issufficient justification for action, for example, ‘When naturalbalances are disturbed by humans, we become ethicallyobligated to assume the mantle of intensive managers’ (56). Thesecond question relates to the feasibility of managing disease infree-living animals. The primary concern of most physiciansand veterinarians has been the diagnosis and management ofdisease in individuals or small groups of individuals.Medication and treatment play an important role in this form ofdisease management. Management of disease in wild animals isusually conducted at the population level where individualtreatment is largely impractical. This has led to scepticism aboutthe feasibility of altering disease in free-living species. However,most advances in public health that have resulted in a greatextension in human life expectancy, and in the health ofdomestic animals, have resulted from improved nutrition,sanitation, provision of safe drinking water and betterhabitation. In the first major book devoted to wildlifemanagement, Leopold noted that in wild animals ‘the realdeterminants of disease mortality are the environment and thepopulation’ (54). Management of environmental factors toimprove nutrition, sanitation, water quality and other habitatfactors, together with manipulation of host populations, ispossible in many wild populations, so that management ofmany diseases may be feasible.

Disease management can be classified into four basic categories,namely: prevention, control, eradication and doing nothing(laissez-faire).

– Prevention includes all those measures designed to exclude orprevent the introduction of a disease into unaffected individualanimals within a population or into an unaffected population.

– Control applies to activities designed to reduce the frequencyof occurrence or the effects of an existing disease within anindividual animal or a population to an acceptable or tolerablelevel, or to contain the spatial spread of infection. Managementof this type implies that some level of disease will persist in thepopulation and that in most instances the control measures willhave to be continued in perpetuity.

– Eradication involves the total elimination of an existingdisease.

– Laissez-faire or not attempting active management has beenthe most common approach to diseases of wild animals in thepast, and may be the most appropriate method when thefeasibility and probability of success of other options have beenconsidered.

The choice among these four basic techniques depends uponwhy management is required, whether or not the disease isalready present in the area or population, the availability of

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techniques for detecting, diagnosing and managing the disease,the availability of funding on a continuing basis formanagement, and the likelihood of success. Selection of themost appropriate technique requires a clear understanding ofthe cause and ecology of the disease, including the course of thedisease in the individual, and the population biology of theparasite-host interaction.

Concepts related to host-parasite relationships have beendeveloped that are important to consider in the planning stageof any potential disease management strategy. Three suchgeneral concepts relate to the population biology of differentforms of disease. An important point in the evolution ofthinking in this area was division of parasites into two broadclasses based on their population biology and the nature of theinteraction between the parasite and the host, rather than onconventional taxonomic status (3).

MicroparasitesMicroparasites are parasites that have direct and usually rapidmultiplication within the host. They are generally small in sizeand have a short generation time compared to the life-span ofthe host. The microparasite group includes most viruses andbacteria, as well as many protozoa and fungi. Infections areusually transient or short-lived and hosts that recover frominfection usually have immunity to reinfection that persists foran extended period. Based on these features, the hostpopulation for a microparasite can often be divided into threedistinct categories, as follows: susceptible, infected andrecovered-immune individuals.

MacroparasitesMacroparasites include parasites that have no directreproduction within the definitive host. These organisms aretypically larger than microparasites and the generation time isextended, often being a considerable portion of the host life-span. The group includes most helminths and arthropods.When immunity develops to macroparasites, it usuallydepends on the number of parasites present and is of shortduration if the parasites are removed, so that infections aretypically persistent and reinfection is common. The distinctionbetween infection and disease is particularly important formacroparasites, because the pathological effects on the host, thesurvival rate of individual parasites in the host and the immuneresponse all depend on the number of parasites in theindividual host. Infection with a few parasites may result in nodetectable harmful effect, while infection with many parasitesmay produce morbidity or death of the host. Categorisation ofthe host population is much more complex than formicroparasites, because of the need to consider the distributionof the parasites within the host population and the varyingdegree of immunity to reinfection that occurs in individuals.

The rate at which a parasite multiplies and increases within thehost population is important for disease management. Thebasic reproductive rate (Ro) has been defined as the average

number of successful offspring that a parasite is capable ofproducing (4). In the case of microparasites, Ro is the averagenumber of secondary infections produced when one infectedindividual is introduced into a host population in which everyindividual is susceptible. For macroparasites, Ro is the averagenumber of female offspring produced throughout the lifetimeof a mature female parasite which themselves achievereproductive maturity in the absence of density-dependentconstraints (4). For any parasite to be maintained within apopulation, Ro must equal at least 1 (i.e. at least one newinfection in the case of a microparasite or one surviving femaleoffspring in the case of a macroparasite). The greater themagnitude of Ro, the more likely the disease may spread withina population.

The host population size required for a disease to becomeestablished and to persist is also an important factor whenconsidering disease management strategies. The size of the hostpopulation has a direct effect on the likelihood of parasitetransmission and, hence, on the magnitude of Ro. Everyparasite requires a minimum number or density of hosts tobecome established. The population threshold forestablishment is often referred to as ‘NT’ and at this level, Ro = 1. In very general terms, the magnitude of NT variesinversely with the efficiency with which a parasite istransmitted. In other words, the more efficiently a parasite istransmitted, the smaller the population required for itspersistence. This can be illustrated by considering infectiousdiseases of canids. Many microparasites, such as caninedistemper virus, produce transient disease with a short periodduring which transmission may occur, do not persist for longin the external environment and require close contact amongindividuals for infection. Although canine distemper spreadsrapidly in a susceptible population, this type of parasite hasrelatively inefficient transmission over the long term and a largehost population is required for Ro to remain >1. When caninedistemper is introduced into a naïve population, some infectedindividuals may die and other infected animals recover andbecome immune. Thus, the number of susceptible individualsin the population decreases. If the population is not largeenough to give birth to sufficient new susceptible animals toreplace those that died or have become immune, Ro will fallbelow 1, and the disease will die out. In contrast, manymacroparasites, such as helminths, have a very long life-span inthe individual host, and the transmission stages are persistentin the environment or in intermediate hosts. Transmission isefficient and the threshold density of hosts needed to maintainthe parasite can be small. Thus, parasites such as intestinaltapeworms, are able to maintain themselves in smallpopulations among which there is infrequent contact betweenindividuals, as is common in carnivores.

Infectious agents can also be classified in another manner thatis useful in considering disease management. Yekutiel dividedagents into endogenous and exogenous groups (103).

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Endogenous agentsEndogenous agents are those that are often present in the bodywithout causing obvious disease, or that are ubiquitous in theexternal environment and that cause disease only under specialcircumstances. Such agents, also called opportunistic orfacultative pathogens, often produce non-specific infections ofthe respiratory, alimentary, urinary and reproductive systems inanimals compromised by other factors.

Exogenous agentsExogenous agents are not present in the body of healthyindividuals but are acquired from outside sources, usually fromother animals. They tend to produce well-defined diseaseshortly after introduction into the body and most do notsurvive for an extended period in the external environment.This simple division is useful because, in general, the morepotential sources that exist for a disease agent, the more difficultit will be to reduce or eliminate the disease. Thus, endogenousdiseases are more difficult to eliminate than exogenous diseases.Yekutiel concluded that eradication, even on a local basis,would only be possible for strictly exogenous diseases inhumans (103).

Although the magnitude of Ro and NT are not known for mostdiseases in wild animals, the goal of management is often toreduce Ro to <1, so that the disease will die out. This might bedone in several ways, for instance by attacking the agentdirectly, by blocking transmission among animals, or byreducing the population of susceptible individuals below NT.The concepts discussed above provide guidance on which typeof management is more likely to be successful in reducing oreliminating a disease. Based on these general principles, onecan conclude in advance that:

– diseases with only one source are more easily controlled thanthose that have multiple sources

– immunisation is more likely to be effective in dealing withdiseases caused by microparasites than for those caused bymacroparasites

– management of disease caused by macroparasites might bedirected at maintaining low levels of infection in the animals toprotect them against damaging heavy infections

– population reduction is more likely to be effective as amanagement strategy for diseases with inefficient transmissionthan for diseases that will persist at very low population levels

– population reduction is unlikely to be effective as amanagement strategy for a parasite that occurs in severalspecies, because the disease may persist in the target speciesalthough the population is below NT, if the parasite ismaintained in other more numerous species.

Indigenous or exotic agentsFinally, infectious agents may be classified as indigenous orexotic (alien) agents. In the case of indigenous agents, an

evolutionary tolerance has generally developed between hostand parasite over millennia, resulting in relative ‘endemicstability’. This stability may be disrupted by human-inducedchanges, such as habitat degradation, fragmentation or loss. Inthe case of alien agents entering an ecosystem, the wildlifepopulations are frequently immunologically naïve, resulting indestructive outbreaks of disease.

Different types of disease will require different disease strategiesand different methods may be employed at specific points in amanagement programme. The various management techniquesavailable have been divided for discussion into reactive, pro-active and population density management. Within each, thebasic elements of prevention, control, eradication and laissez-faire apply.

Reactive disease strategiesThis group of techniques is applied in circumstances in whicha disease is present in an area or population of animals, and thedesire is to either reduce its impact (i.e. contain and control thedisease), or to eliminate it completely. Management can beaimed directly at the disease agent, at reducing transmission, orat preventing access to the disease agent.

Disease agents can be ‘attacked’ within the host animal, free inthe external environment, or in some vector or alternate host. Ifthe disease has only one vertebrate host, or transmission islimited to some identifiable part of the external environment,attack on the agent may be a feasible strategy. The morepotential sources that exist for the agent, the less likelymanagement directed at the agent per se will be successful.

Destruction of the parasite within the vertebrate host throughuse of drugs such as antibiotics or anthelmintics is commonlyused to control disease in humans and domestic animals. Adisadvantage of this approach is that the parasite may alreadyhave caused injury to the host before treatment. There is noreason to believe that this method would not also be useful inwild animals, if appropriate drugs could be delivered to theindividuals. However, the basic problem lies in finding amethod of delivering treatment to the animal. It is for thisreason that treatment has limited application in wild animalsexcept, perhaps, in isolated groups such as endangered speciesin which affected individuals can be identified and captured fortreatment. For example, Bornstein et al. reported that sarcopticmange was treated successfully in a small population of Arcticfoxes (Alopex lagopus) in Sweden by capture, treatment andrelease (15). Similarly, individual red grouse (Lagopus lagopusscoticus) were captured on British moors and treated with ananthelmintic to reduce infection with the nematodeTrichostrongylus tenuis (28, 49). Treated females producedsignificantly more young than did untreated females. Thisexperimental treatment was conducted on study areas up to800 ha in size, but the feasibility of using the technique moreextensively has not been reported.


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A programme to control psoroptic mange in a small remnantpopulation of desert bighorn sheep (Ovis canadensis nelsoni) inNew Mexico illustrates several problems in using individualanimal treatment as a method of disease management (53).When the disease was recognised in 1978, the populationcontained 200-250 animals but declined to <70 by 1979. Thedecline was thought to be due to mange. Initially, acaricide wasplaced in bags over salt blocks in the hope that the sheep wouldbe dusted with acaricide while using the salt. However, sheepavoided the bags. (Techniques used to deliver treatment todomestic species may fail in wild animals because of differencesin behaviour). Next, as many of the sheep were captured aspossible, dipped in acaricide solution, held in captivity for 10to 14 days, re-dipped, and then transferred to a holding areawhere they were maintained for about a year until released. Thecost to capture and treat each sheep was about US$2,000 (53).(This type of treatment is feasible only for small numbers ofhighly valued animals. Often, as in this situation, the entirepopulation cannot be captured for treatment.) This treatmentapparently was successful in removing mites, although nosensitive diagnostic technique was available to detect low-levelinfections. Only 59% of the treated animals survived treatment.(Capture and handling of wild species for treatment may resultin unacceptable mortality.) Animals that could not be capturedwere injected remotely with anthelmintic by airgun from ahelicopter. The programme was judged to have been successfulin controlling but not eliminating the disease; however, mangerecurred and treatment was changed to capture of visiblyaffected sheep for treatment. It was concluded that continuedannual treatment would be necessary (70). In this example, theagent was a macroparasite with features of an endogenousagent, in that lightly infected sheep had no clinical signs. Evenif treatment was successful in eliminating mites from individualsheep, recovered animals would not have long-lastingimmunity and re-infection could be expected. The NT for thisparasite is probably very low, so that the parasite could persistin a very small population, with a few infected individualsserving as a reservoir for reinfection of treated animals.

A study by Murray et al. is important in the discussion ofindividual animal treatment as a management option, becauseit provides detailed information on the efficacy of anthelmintictreatment in reducing parasites in a wild population (65).Snowshoe hares (Lepus americanus) were captured and treatedbimonthly with the anthelmintic ivermectin. The prevalenceand intensity of infection with five nematodes and one speciesof tick were compared between treated and untreated haresover a 27-month period. Treatment significantly reduced themean prevalence of infection by four of the nematodes and themean intensity of infection by three nematodes but sometreated hares showed no reduction in either prevalence orintensity of infection compared to control animals. Treatmentreduced the prevalence of two nematodes for about 50 daysand longer for two other species. Treatment had no effect on thetick Haemaphysalis leporispalustris. Based on the large variationin effect among individuals and the short duration of effect,

Murray et al. stated that it ‘remains questionable to what extentanthelmintics may be used for the conservation or managementof wild populations’ (65). Considering the difficulty indelivering drugs repeatedly, they concluded that ‘it may neverbe possible to successfully implement long-term nematodecontrol in free-ranging populations exclusively viachemotherapeutic drugs’.

Treatment of individual animals can and should be used toreduce the risk of translocating disease agents in wild animalsbeing moved to new environments; however, it must not berelied upon as the sole method of preventing transfer of diseaseagents. For example, the nematode Elaphostrongylus cervi wasintroduced to Australia (73) and the tick Dermacentor albipictuswas introduced to New Zealand (42) with cervids that had beentreated prior to translocation. Part of the problem in this regardis that the drugs that might be used have often not been testedextensively in wild animals, or against parasites of wild animals,so that their actual efficacy is unknown.

Widespread or mass medication has been attempted for a fewhuman diseases, including malaria and schistosomiasis.Development of acquired resistance by the parasite to thechemical used is a definite risk in any programme that isdependent upon continued and widespread use ofchemotherapy because of the selective pressure for resistantorganisms. The other major problem with this technique lies indelivery of the treatment to the individual, even in humans.There have been very few attempts to use mass treatment inwild animals. Anthelmintics were used to controlProtostrongylus spp. lungworms in bighorn sheep (Oviscanadensis) on a few occasions (85). Sheep were accustomed toconsuming bait to which anthelmintics could be added.Treatment was timed to kill larval parasites in pregnant femalesand reduce transplacental infection of lambs in utero. It was alsohoped that treatment would reduce the number of adult wormscarried by sheep and, hence, environmental contaminationwith larvae. While the survival rate of lambs from treated eweswas much higher than that of lambs born to untreated ewes(85), treatment did not eliminate lungworms from thepopulation nor did it deal with the underlying problem of toomany sheep concentrated on small areas of heavilycontaminated habitat. Miller reported that anthelmintic therapyhad failed to prevent epidemics of pneumonia in bighorn sheeppopulations in Colorado (61). The same method of baiting wasused to deliver antibiotics to groups of sick sheep during apneumonia outbreak (33) but the effectiveness of this treatmentis unknown. Qureshi et al. reported that anthelmintics could bedelivered to free-ranging white-tailed deer (Odocoileusvirginianus) using a baiting system (76). The objective in thiscase was to control transmission of the liver fluke Fascioloidesmagna among deer and thus prevent contamination of pastureand infection of cattle. Over a three-year experimental period,the prevalence of the parasite in treated deer on a 391 ha studyarea was reduced to 8.7% compared to 72% on control areas.The feasibility of applying this technique over larger areas is


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unknown, as is the risk of acquired resistance if theanthelmintic were to be used repeatedly over a wide area.

If a disease agent is localised in a specific site in the externalenvironment, it may be possible to destroy it there and reduceor prevent infection. Collection and disposal of carcasses ofanimals that have died of disease is a method that has beenemployed frequently for disease occurrences in wild animals.Friend and Franson provide detailed instructions on methodsfor collecting and disposing of carcasses of small animals (birds)(35). Disposal of carcasses to reduce contamination andtransmission seems intuitively sound, because carcasses maycontain infectious organisms. However, there are noquantitative data to indicate the degree of carcass sanitationrequired to reduce the incidence of any infectious disease. Theeffectiveness of carcass sanitation has been studied in regard toavian botulism. While botulism is not an infectious disease,toxin formed within bird carcasses propagates the disease,mimicking an infectious process, so the results of studies maybe relevant for infectious conditions. Reed and Rocke foundthat sentinel ducks (Anas platyrhynchos) in experimental penscontaining carcasses were significantly more likely to developbotulism than were ducks in pens with no carcasses (77). Thisconfirmed that carcasses are an important source of toxin andthat complete removal of all carcasses would be a soundmanagement technique. In natural situations, it may be difficultor impossible to find and remove all carcasses. For instance,only 6% of duck carcasses placed in a Texas marsh weredetected by searchers (93) and 32% of marked carcasses wererecovered in carcass collections during a botulism outbreak inSaskatchewan (21). The proportion of carcasses collectedduring clean-up operations during an intensive study ofbotulism in prairie Canada ranged from <10% on large, heavilyvegetated lakes to approximately 60% on intensively searchedsmall wetlands. In this study, there was no improvement insurvival of radio-marked ducks on lakes with carcass clean-upcompared to similar lakes on which no carcasses were collected(T. Bollinger, personal communication). The value of carcasssanitation is likely to be disease- and site-specific. It will varywith the persistence of viable infectious agents within carcasses,the amount of contact between live animals and carcasses, andthe dose of organisms required for infection, as well as the easewith which carcasses can be found and the effort devoted tocarcass collection.

Disinfection and other forms of sanitation are used frequentlyin human and veterinary medicine. Disinfection has been usedin a number of circumstances involving infectious diseases ofwild animals, including treating waterholes associated with thetransmission of anthrax (71), disinfecting wetlands where aviancholera (37, 84) and duck plague (68) were occurring inwaterfowl, liming to destroy parasite eggs around artificialfeeding sites used by hares (88), and disinfection of soilenriched by bird droppings in which the fungus Histoplasmacapsulatum was known to grow (101). The effectiveness ofdisinfection in reducing or preventing infection seldom has

been evaluated, however, Skrjabin reported that lungworms(Protostrongylus spp.) were eliminated from hares after threeyears of liming around feeders, while hares in untreated areasremained infected (88). Disinfection is only practical insituations in which the agent or transmission of the diseaseoccurs in a very limited area. Another potential problem is thatthe chemicals required may have undesirable environmentaleffects that preclude their general use. Disinfection should beconsidered as a component of the management programme forsituations in which wild animals have to be concentrated, suchas at artificial feeding or watering sites.

Habitat modification to destroy agents or to interfere withdisease transmission is potentially of great value in diseasesaffecting wild animals. Application of these methods requires athorough knowledge of the ecology of the disease to beeffective, and there are few specific examples available of thesuccessful use of this type of management for diseases ofwildlife. The ‘tools’ for this type of management are oftensimilar to the axe, fire and plow that Leopold suggested couldbe used to ‘doctor’ wild animal diseases (54). Fire is a powerfultool for habitat manipulation and has been used occasionally indisease management. Pienaar burned vegetation in areas whereanthrax occurred to destroy the bacterium and to facilitatefinding carcasses (71). Under experimental conditions, burningreduced the number of ticks parasitising young wild turkeys(Meleagridis gallopava) (50) and prescribed burning of forests iseffective in reducing populations of several species of tick (1).Seip and Bunnell (87) reported that Stone’s sheep (Ovis dallistonei) grazing on ranges burned annually passed lesslungworm larvae than did sheep using unburned range, butwhy this occurred and the significance of this observation areunclear. Habitat manipulation of another type was performedto reduce water-borne transmission of Pasteurella multocidaamong eider ducks (Somateria mollissima) in the St LawrenceRiver, Canada (102). Avian cholera occurred repeatedly amongnesting birds on one island while it did not occur among birdson adjacent islands. The problem island was heavily shaded byvery dense shrub cover and had poor drainage with standingwater, from which P. multocida was readily isolated. Theunaffected islands were open, grassed and well-drained. It washypothesised that transmission was occurring in associationwith the standing water, so the shrubs were cleared, thestanding water was drained and grass was planted. The islandcontinues to be used by breeding eiders and avian cholera hasnot occurred at high levels since the habitat was modified.Waterholes were modified in dry areas of California to reducethe occurrence of necrobacillosis among deer (83). Theobjective was to prevent concentration of animals in areascomposed of ‘mud, contaminated by droppings’ that wereheavily contaminated with the causative bacterium. It wasthought that animals became infected by walking through themud at these sites and subsequently developed pododermatitis(footrot). Management consisted of filling and covering somewaterholes, reducing overflow from water tanks to reducemuddy conditions, and creating new clean water sources.


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Habitat modification is more often directed at either thevertebrate or invertebrate hosts of disease than at the causativeagent per se. For example, fire may have more value as amethod for influencing animal distribution than in destroyingdisease agents. Pienaar felt that burning helped to limitgeographical spread of anthrax by keeping animals in theoutbreak area to graze on the regrowth that occurred after thefire rather than dispersing to new areas (71). Environmentalmanipulation may range from simple, localised changes, suchas filling tree holes to prevent their use by breeding mosquitosthat transmit viral diseases (62), locating woodpiles androckpiles away from dwellings to reduce contact betweenhumans and rodents that carry hantaviruses and Yersinia pestis,and mowing lawns around dwellings to reduce ticktransmission of Lyme disease from wild animals to humans, towidespread landscape alterations. An example of the latter typewas the clearing of riverine vegetation that formed essentialhabitat for tsetse flies (Glossinia spp.) as part of a programme tocontrol diseases transmitted between wild and domesticanimals (38). Habitat modification may be used to disperseanimals away from known disease sites, for example bydraining wetlands where outbreaks of botulism and aviancholera occur and fencing waterholes to prevent access duringanthrax outbreaks. This is often most effective when suitablenew alternative habitat is created. Habitat modifications mayalso be used to encourage animals to use areas of lower risk.Skrjabin described construction of artificial watering sites tocontrol infection of moose (Alces alces) by a damagingtrematode (probably Parafasciolopsis fasciolaemorpha) (88). Thisparasite is transmitted by snails that were abundant in wet areasused by moose in dry years. Ponds were dug in peat bogs wherethe snails were absent because of the acidity of the soil andwater. Moose using these ponds were parasitised much lesscommonly than those using natural, less acidic, waters.

The term ‘vectors’ is used here to mean invertebrates that carryor transmit an infectious agent between vertebrates. Vectorsmay be either required or a facultative part of the ecology of adisease. Manipulation of vectors is an important part of themanagement of many diseases in domestic animals andhumans. This has usually been done by attempting to reducethe population of the vector species. Some general features ofvectors should be considered when vector control iscontemplated, as follows:

– prevalence of infection in the vector is usually extremely lowcompared to that in the vertebrate host (i.e. the great majorityof the vector population is not infected)

– the life-span of most vectors is very short, and they often havethe ability for very rapid increase, so that populations mayrebound rapidly after reduction

– the activity of many vectors is highly seasonal and is affectedby weather, so that they may be available for control onlyduring a restricted period

– species responsible for disease transmission often compriseonly a tiny proportion of the population of similar species thatmay be harmed by any control programme.

The introduction of highly effective pesticides led to a belief thatmany diseases could be controlled or eliminated by vectorpopulation reduction using these chemicals. However, twomajor problems were recognised early and continue to limit theeffectiveness of this management method. The first is that manycompounds suitable for killing vectors are broad-spectrumpoisons with serious environmental side-effects that limit theirusefulness. The second is that acquired resistance developsrapidly in vector populations following the repetitive use ofchemicals. For these reasons, chemical control of vectors hasoften been unsuccessful.

There have been few attempts to control vectors that carrydisease of wild animals, except in the case of zoonotic diseases.Insecticides, including DDT (dichloro-diphenyl-trichloro-ethane), carbaryl and permethrins, have been used to controlfleas involved in transmission of Yersinia pestis among wildrodents (10, 11, 36), including intervention in outbreaks ofplague among black-tailed prairie dogs (Cynomys ludovicianus)(36), the principal prey of the endangered black-footed ferret(Mustela nigripes). General area-wide distribution of insecticidefor this purpose has been unsuccessful and acquired resistancehas been observed (10). Even targeted application of insecticideto burrows resulted in a ‘significant problem’ … ‘through killingnontarget insect species with associated ramifications to theecosystem’ (36). Copper sulphate was used to kill aquatic snailsthat were the intermediate host for the liver fluke Fascioloidesmagna in the former Buffalo National Park, Alberta, Canada(94). Pybus concluded that this technique was successful ineradicating the fluke, but that ‘considering the greatenvironmental impact of such methods, they are unlikely to beused in a modern situation’ (75). Several acaricides have beenused extensively on lawns around homes in some areas toreduce populations of Ixodes dammini, the tick that transmitsLyme disease from wild animals to humans (91). In general, itappears that pesticides are most useful when used in a veryselective manner in small areas and in combination with othermethods including environmental manipulation and biologicalcontrols.

Pro-active managementThis group of techniques includes those intended to preventintroduction of a disease agent into an area where it does notoccur, and those designed to protect individual animals fromeither infection or disease.

Infectious diseases have a geographic range that is determinedby the presence of adequate suitable host animals, i.e., a hostpopulation > NT, and by a variety of environmental factors thatallow transmission of the infectious agent. The geographicrange of a disease can be viewed as being constrained by anecological ‘barrier’ that consists of many components. The


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range of an infectious agent may increase and new areas may becolonised as a result of natural phenomena that alter theecological barrier, such as increased rainfall or changes invegetation, or in response to human-induced changes. Humansmay alter ecological barriers allowing a disease agent to extendits range or completely circumvent existing barriers. Examplesof the former type range from global effects, such as climaticwarming, to local effects such as irrigation providing newhabitat for disease vectors, concentrating animals throughfeatures such as artificial feeding, or by altering otherenvironmental factors that change the distribution andabundance of animals. Ecological barriers are circumvented bydirect translocation of infectious agents or more commonlythrough moving animals together with their disease agents.

Management to prevent movement of an infectious disease andits spread into new areas should be viewed as a process ofprotecting or supplementing natural ecological barriers, or ofreplacing natural barriers with artificial barriers. As it is difficultor impossible in the long-term to prevent natural changes, thistype of management is usually directed at human-inducedchanges and consists of modifying human behaviour. This mayinclude altering existing activities as well as considering thepossible consequences of new activities on disease during theplanning stages. Reducing or preventing global changes such asclimatic warming go far beyond management of disease in wildanimals, but local ecological barriers may be managed.

The most direct form of barrier management are measuresdesigned to prevent the translocation of disease agents and/ordisease vectors. Translocation of wild animals is a commonmanagement tool and has been used both to introduce newspecies and to restore extirpated populations. However, thereare many historical examples of translocation of diseases ofwildlife. Some of these were intentional, such the introductionof myxomatosis and rabbit haemorrhagic disease into Australia,but most were inadvertent, for instance the introduction ofboth the causative agent and the vector mosquito of avianmalaria into Hawaii, introduction of F. magna with elk fromNorth America to Europe, translocation of raccoon rabiesnorthwards in the United States of America (USA), andintroduction of nematodes of the genus Elaphostrongylus incervids moved from Europe to other continents. In the past, therigours of transport and the time required to move animalsserved as an unintentional barrier to translocation of diseaseagents, since many hosts, vectors and disease agents failed tosurvive the trip. However, the risk of such introductions hasincreased dramatically because of developments intransportation. The short travel time between any two pointson the globe at present is often less that the incubation periodfor many infectious diseases.

The potential for disease movement through animaltranslocation and reintroduction has been discussed by several

authors (8, 23, 24, 39, 45, 66, 102). Any animal translocationcontains two types of risk, as follows:

a) that the introduction of exotic disease with the animals mayadversely affect indigenous animal populations at the releasesite, and

b) that diseases present in the indigenous animals at the releasesite may have adverse affects on the translocated animals.

Corn and Nettles referred to the latter as a ‘reverse risk’ (23). Inthe light of these two types of risk, animals should never betranslocated without a thorough understanding of the potentialdisease agents present at both the site of origin and the releasesite. A critical factor that must be considered in any proposedtranslocation and release of wild animals is that living animalscannot be sterilised. At least some of the microfauna that occurin and on any animal will be moved with the animal. Davidsonand Nettles used the term ‘biological package’ to describe theanimal, together with its infectious agents and parasites that itmoved (24).

Corn and Nettles proposed a protocol to reduce the disease riskassociated with translocation of elk in North America (23). Theprotocol contains five components that are applicable to anyproposed translocation or reintroduction of wild animals, asfollows:

1. Evaluation of the health status of the source population. Thisshould include a complete review of all available informationon the health of the source population, as well as testing of asignificant sample of the population for specific diseases, usingserology and necropsy where appropriate.

2. Quarantine of the animals that are to be moved to allowtesting and observation. To be effective, the quarantine periodmust be at least as long as the maximum incubation period forany known disease of concern.

3. Physical examination and diagnostic testing of animals to bemoved. While this will reduce the risk of disease transfer, itmust be remembered that no pre-movement test is likely to be100% effective in detecting every infected individual.

4. Restriction on translocation from certain areas or populationswhere specific diseases are known to occur. This is particularlyappropriate for diseases for which there is no reliable liveanimal test (e.g. chronic wasting disease of cervids).

5. Prophylactic treatment of the animals to be moved.Chemotherapy will reduce the likelihood of transferring certaindisease agents, but treatment is unlikely to be 100% effective inremoving infectious agents from infected animals. This isparticularly true for wild species for which there is usually littleor no information available on appropriate dosage of drugs, orthe efficacy of the drugs that might be used.

In addition, the health status of animals at the release site mustalso be evaluated. This should include a review of all species,including domestic animals, that might be susceptible todisease agents that could be introduced with the translocation,


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as well as species that might carry agents that could potentiallyharm the introduced animals.

Despite all of these precautions, there is always a risk in anymovement of animals that disease agents that are currentlyunrecognised may be translocated, become established, andcause disease problems in the new area.

The development of effective vaccines and mass immunisationhas had dramatic effects on many infectious diseases of humansand domestic animals. There is no reason to think thatimmunisation would not be similarly effective in wild animals,if appropriate vaccines were available and could be delivered tothe animals. Although the use of immunisation has beenrestricted to a small number of diseases of free-living animals,there is good evidence that it may be very effective undercertain conditions.

The purpose of immunisation is to render the individualresistant to an infectious agent. This resistance may be of twotypes. It may prevent the animal from becoming infected, or itmay prevent the development of disease. It is very important todistinguish between these two forms of resistance, becauseanimals immunised with a vaccine that prevents disease but notinfection may still be able to transmit the causative agent. Theobjective in immunising animals may also be of two types. Insome instances, the objective is to protect the individual fromthe disease. For example, immunisation was used to preventanthrax in roan antelope (Hippotragus equinus) in Africa (27)and bison (Bison bison) in Northern Canada (20). Bacillusanthracis is present in the soil and there is little or no directtransmission from infected individuals to susceptible membersof the population so that the aim in these programmes was toprevent animals from dying of the disease rather than to reducetransmission of the causative agent. In contrast, immunisationof wild carnivores including foxes (Vulpes vulpes), stripedskunks (Mephitis mephitis) and raccoons (Procyon lotor), isdesigned to reduce transmission of the disease within thepopulation, although immunisation also protects theindividual. Obviously, a vaccine that prevented development ofdisease but not infection and transmission would be lesssuitable than one that prevented infection, if the goal is toreduce transmission. Immunisation designed only to protectthe individual animal is likely to be of limited usefulness in free-living animals except in circumstances, such as management ofendangered species, where the cost of delivering vaccine can bejustified. The remainder of the discussion will deal with massimmunisation designed to reduce transmission.

When the goal is to decrease transmission of a disease,immunisation is used to reduce the proportion of susceptibleanimals in the population. In diseases caused by microparasites,the population can be sub-divided into susceptible, infectedand resistant components and that immunity induced byinfection or immunisation tends to be long-lasting. In contrast,immunity in diseases caused by macroparasites depends on thenumber of parasites present, is short-lived when no parasites

are present, and reinfection is common. For these reasons,immunisation is more likely to be effective as a managementstrategy for reducing transmission of diseases caused bymicroparasites than of diseases caused by macroparasites.

The proportion of the population that must be immunised tohave a significant effect on disease transmission is related to Ro,the reproductive rate of the disease. In general, the proportionof the population that must be immunised must exceed 1-1/Ro(2), so that a large proportion of the population must beimmunised in those diseases in which each infectiousindividual results in infection of many susceptible members ofthe population. Because Ro is related to population density, ingeneral, the greater the population density, the larger theproportion of the population that must be immunised fordisease control. Populations with a high recruitment rate andrapid turnover have a high proportion of new susceptibleanimals and may require high rates of immunisation to beeffective.

An important factor in any immunisation programme is theaverage age at which susceptible animals are exposed to thedisease agent. To be successful, immunisation must occur priorto infection, so that the average age of immunisation must beyounger than the average age of infection in the population. Ingeneral, diseases in which animals are exposed at an early agewill be more difficult to control through immunisation thandiseases with a later average age of exposure. Diseases that aretransmitted vertically from dam to offspring, or in whichtransmission occurs before there is any opportunity forimmunisation, e.g., transmission before emergence from theden, are probably not amenable to management throughimmunisation. In some diseases there may be only a narrowwindow of time during which immunisation would be effectivebetween the decline of maternal (passive) immunity in younganimals and the average age of infection. Cassier et al.experimented with immunisation of female bighorn sheep toprotect their offspring from pasteurellosis (19).

The other essential features of any immunisation programmerelate to the characteristics of the vaccine and the ability todeliver the vaccine to a sufficiently large proportion of thepopulation. Desirable features of a vaccine include thefollowing requirements:

– it produces no significant disease in the host or non-targetspecies

– it stimulates long-lasting protective immunity (preferablyafter a single exposure because of the difficulty of deliveringrepeated doses of vaccine to wild animals)

– it is protective against all varieties of the causative agent in thearea

– it is incapable of reversion to a pathogenic form

– immunised individuals can be differentiated from animalsrecovered from natural infection

– it is inexpensive and stable.


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Wobeser has discussed requirements of vaccines in detail (102).

In most situations related to wild animals, it is not practical tocapture and handle individual animals for immunisation;however, this may be possible for small numbers of highlyvalued animals or in other special circumstances. For instance,De Vos et al. (27) used a helicopter and dart gun to vaccinateindividual roan antelope to protect them from anthrax andCassier et al. (19) vaccinated bighorn sheep captured with ahelicopter and netgun. Rosatte et al. (80) reported thattrapping, vaccinating and release of skunks and raccoons wasan effective method of controlling rabies in an urbanenvironment, and this technique also was used to createbarriers to the spread of raccoon rabies in Ontario, Canada(81). Elk have been immunised for brucellosis on feedinggrounds in Wyoming, USA, using a ‘biobullet’ (89). Between1965 and 1977, almost 28,000 bison in northern Canada wererounded up in corrals with helicopters and vaccinated againstanthrax (96). The effectiveness of the latter programme has notbeen assessed.

The most effective method for mass immunisation of wildanimals is through distribution of oral vaccine that is effectivewhen ingested with a bait. For this purpose, vaccines must havefeatures in addition to those listed earlier. First, the vaccinemust produce immunity when ingested. Second, because thevaccine is placed in the environment, it is imperative that itmust be non-pathogenic for non-target species that mightinadvertently ingest the bait. Third, the vaccine must be stableand retain its immunogenicity for as long as possible underadverse environmental conditions. Given the different foodpreferences and foraging habits of the different species,extensive testing is usually necessary to develop a bait that isvery attractive to the species being targeted and less attractive tonon-target species (31). Baits consumed by non-target animalsare wasted and it may be difficult to deliver sufficient baits tothe target species if there is strong competition with many non-target animals (92). The appropriate bait density for a particularsituation must be discovered through testing in which theproportion of the target population consuming one or morebaits and the proportion of the population developingprotective immunity are measured. The frequency of baitingrequired varies among species, and among locations for thesame species (58). As the Ro is not known for diseases of wildanimals, and is highly variable from situation to situation, it isnot possible to predict the proportion of the population thatmust be immunised to control a disease. Oral vaccination,using a variety of vaccines, baits and methods of delivery, hasbeen successful in eliminating rabies from foxes in severalEuropean countries and in Ontario, Canada (58). This methodmay be practical for other diseases in which the high costs forvaccine and bait development and testing, and the relativelyintense effort required for bait delivery can be justified.

In summary, immunisation is best suited as a managementstrategy for microparasitic exogenous infections that have a low

reproductive rate, in populations with a low turnover rate andin which the average age of infection occurs later in life. Captureand handling of animals for parenteral administration ofvaccine is likely to be practical only for valuable species onsmall areas or under other unusual circumstances. Massimmunisation with oral vaccines delivered in bait may beeffective, but its use is likely to be limited to a few seriousdiseases, because of the cost of developing, testing anddelivering appropriate vaccine-bait combinations.

Population density management for diseasemanagementPopulations of host animals can be manipulated in severalways, with the objective of reducing disease transmission oreliminating the disease agent from a population. Thetechniques can be divided into four broad categories, asfollows:

– alteration of animal distribution

– selective removal of diseased animals from the population

– general reduction in population density

– elimination or eradication of the total population that mayhave been exposed to the disease.

These categories can be considered as a series of steps in whichthe intensity of the action, the violence on the population, andthe probability of public resistance increase with each step.

The objective in changing the distribution of animals for diseasecontrol is usually to reduce contact between susceptible andinfected animals, or between susceptible animals and somespecific geographical feature where transmission occurs. Thistechnique is applicable only where the disease is limited to anidentifiable area or site. A common recommendation in the faceof a localised disease outbreak or epizootic, particularly amonghighly mobile species such as birds, is to disperse the animalsaway from the site. This technique has been employed tomanage outbreaks of avian botulism (67), and to movewaterfowl away from an outbreak of duck plague (68) andwhooping cranes (Grus americana) away from an avian choleraepizootic (104). Pienaar discouraged vultures from usingwaterholes and destroyed vulture roosting sites to preventcontamination of waterholes with Bacillus anthracis carried fromcarcasses of animals dead of anthrax (71). Meagher describedattempts to relocate bison in the Yellowstone National Park aspart of a programme to manage brucellosis and preventtransmission to cattle (60).

It is extremely difficult to move wild animals out of theirestablished range. Techniques used to frighten or haze animalsrapidly lose their effectiveness with continued use (59) andanimals will return or repopulate areas quickly unless thehabitat can be made unattractive or suitable alternative habitatis made available. New attractive habitat may have to be


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created. For example, Parrish and Hunter flooded newwetlands to facilitate moving birds away from a botulismoutbreak (67). Dispersal of animals into new areas also maycreate other management problems in the new area.

The value and efficacy of animal dispersal as a diseasemanagement strategy has never been evaluated in any type ofcontrolled study of a wildlife disease. This technique is bestsuited for dealing with non-infectious diseases, such aslocalised toxin spills, in which there is no risk that moving theanimals will also move the disease agent and establish new fociof disease. When dealing with infectious disease, there may bea risk that some of the animals dispersed will be infected andthat these may establish new foci of infection and, hence,expand the geographical range of the disease. If the disease tobe managed is known to have a very restricted distribution, oris a newly discovered disease, dispersal of animals from theknown areas of infection should not be attempted because ofthe risk of extending the range. However, if the disease agent isknown to be widespread, and the occurrence of clinical diseaseis dependent on some environmental factor limited to aparticular site, dispersal may be an appropriate strategy. Thefirst major outbreak of duck plague among wild birds in NorthAmerica provides a good example of the dilemma associatedwith dispersion. That outbreak, in which about 10,000mallards (Anas platyrhynchos) and several hundred Canadageese (Branta canadensis) died, occurred in mid-winter on asmall area of open water in a refuge in South Dakota (68).Although this was the first major epizootic of duck plaguerecognised among wild waterfowl in North America, and thedisease was considered at the time to be exotic to NorthAmerica, a decision was made to disperse the birds rather thanto try to contain the disease. Although there is no evidence thatthe dispersal of potentially infected birds resulted in widespreaddispersion of the particular virus found at the outbreak site,containment and depopulation would probably have been amore sound strategy (102). Friend and Franson concluded that‘As a general rule, animal dispersal is not recommended wheninfectious disease is involved, unless it can be assured that thepopulation being dispersed will not infect other wildlife’ (35).

Enforced separation of infected and susceptible animals hasbeen used to prevent transmission of diseases between wild anddomestic animals, and in a few instances to separate wildanimals from humans to reduce transmission of a zoonoticdisease. For instance, game-proof fences have been used inAfrica to separate African buffalo (Syncerus caffer) infected withfoot and mouth disease, bovine tuberculosis and theileriosisfrom domestic cattle (44, 51), and wild pigs (Phacochoerusaethiopicus and Potamocheorus porcus) infected with Africanswine fever from domestic pigs (51). Limited fencing acrosstravel routes was attempted to prevent bison potentiallyinfected with brucellosis from leaving the Yellowstone NationalPark and coming into contact with cattle (60). The fences in thelatter instance were ineffective because the bison rapidlydeveloped detours to circumvent the fences. Fencing to exclude

deer resulted in a marked reduction in the number of larval andnymphal Ixodes dammini ticks on small experimental areas in aregion where Lyme disease was endemic, leading Stafford toconclude that fencing of ‘moderate tracts of land’ could be aneffective component in reducing risk of Lyme disease (90).Fences are not feasible for diseases transmitted by highlymobile vectors, or for diseases in which small animals areinvolved as potential hosts of the disease. For example, Staffordfound that rodents introduced ticks through deer-proof fences(90). Fences are relatively expensive to construct, requirecontinual maintenance and periodic replacement, may requireextensive habitat disruption for their construction, mayseriously disrupt the movement of wildlife not affected by thedisease, and are subject to failure. Some forms, such aselectrified fences, may not be acceptable in areas where humancontact is likely. For management of infectious diseases thatmay pass between wild and domestic species, double-fencingwith an animal-free exclusion zone is usually required toprevent close contact between animals. The fence must besufficiently robust and impermeable to prevent movement of allspecies that might be involved in disease transmission orsympatric species that are known to challenge and break fences.For instance, 2-m high fences are sufficient to confine gamefarm elk but do not prevent the entry of wild deer (Odocoileusspp.) into the pens. This became a concern when chronicwasting disease, that affects both deer and elk, was discoveredin elk on game farms. Enforced separation, using methods suchas fences, has relatively little application in management ofinfectious disease among free-living animals, except in verylocal situations, but may have an important function at theinterface between wildlife and traditional agriculture.

Another management technique aimed at reducing oreliminating a parasite from a population is to selectively removeinfected individuals. ‘Selective culling’ or ‘test-and-slaughter’has been used successfully as part of the management strategyfor several diseases of domestic livestock. There are a numberof requirements that limit the application of selective culling foruse in wild animals. It is only appropriate for situations inwhich:

a) the entire population can be examined

b) infected individuals can be identified (i.e. a sensitive andspecific test is available)

c) infected individuals can be readily captured (repeatedly) fortesting

d) animals known to be free of the disease can be isolated fromthe untested portion of the population, and

e) removal or sacrifice of a portion of the population isacceptable or tolerable.

Primarily because of the need to capture, handle and holdindividual animals, this method has not been used widely inwild animals. Test and removal was used in conjunction with


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calfhood vaccination to eradicate brucellosis from a captiveherd of bison in Elk Island National Park, Alberta, Canada (96).Facilities were available in this situation to handle the animalsrepeatedly. All of the original group of animals eventually testedpositive and were destroyed, but some of their offspringremained free of brucellosis and provided the nucleus of a newherd. Selective killing of visibly affected individuals was used,together with chemotherapy through treated salt blocks, tocontrol sarcoptic mange in chamois (Rupicapra rupicapra) (72).Test-and-slaughter was rejected as an option for elimination ofbrucellosis and tuberculosis from a free-ranging population ofbison in Wood Buffalo National Park, Canada, for manyreasons, including the impracticability of capturing over 3,000 wild bison in a 44,000 km2 wilderness, the difficulty inholding test-negative animals so that they would not beexposed to infected individuals that had not been tested, thelack of highly sensitive tests, and the likelihood of a high rate ofinjury and mortality associated with capture and handling(102). Because of the requirements for success, selective cullingis unlikely to be a common method of disease management inwild animals. It might be used as an alternative to totalpopulation elimination in situations where it is imperative toconserve genetic diversity while eliminating a disease.

The reverse of selective culling is being used in northernCanada to develop a population of bison free of brucellosis andtuberculosis, beginning with a wild source herd in which bothdiseases occur at high prevalence. In this approach, rather thanselecting individuals infected with the disease for disposal,individuals with the least likelihood of being infected areselected from the herd and retained. Intensive searches areperformed to locate neonatal calves within the free-living herd.The calves are removed to an isolation facility, treatedintensively with antibiotics, and reared in pairs to reduce thepotential loss should an infected individual be recognised. Theanimals are tested repeatedly during rearing to maturity, andtheir offspring will be used as the foundation of a new herd freeof the diseases. The plan is to remove the free-ranging diseaseherd prior to reintroducing disease-free animals to the wild.Similarly in South Africa, the breeding of African buffalo thatare free of foot and mouth disease, theileriosis, tuberculosis andbrucellosis is currently being successfully practised, to supply‘clean’ buffalo to conservation areas outside the disease endemiczones (12).

Reducing the population of animals within an area has beenattempted frequently as a method to manage disease in wildanimals. Population reduction is based on epidemiologicaltheory that predicts that for directly transmitted infections, theper capita rate of disease transmission and the prevalence ofdisease will increase with increasing population density.Although usually not stated in these terms, the goal is to reducethe population to a level at which Ro approaches 1, so that theincidence of the disease is reduced, or to below NT at whichpoint Ro = <1, and the disease will die out. Populationreduction is most likely to be effective for diseases in which

there is only a single source of infection, and unlikely to beeffective for diseases that occur in several species or that havemultiple sources of infection. Population reduction is morelikely to be effective as a management strategy for diseases withinefficient transmission, than for parasites such as manymacroparasites, that are transmitted very efficiently. The degreeof population reduction required or desired is sometimesexpressed in relation to carrying capacity, which is the densityof population at which birth and death rates balance or atwhich the population is at an equilibrium. While populationsare never likely to truly achieve an equilibrium, and there willbe different equilibrium points under different circumstances,the concept of carrying capacity is useful as a reminder that thepopulation size is a balance between the removal of animalsfrom the population by all causes, including the disease itselfand the depopulation effort, and recruitment to the populationthrough reproduction and immigration. The more intense thedepopulation effort, the lower the reproductive rate of theanimal, and the less recruitment that occurs throughimmigration, the greater the likelihood of effective populationreduction.

Population density could be reduced either by decreasing thenumber of animals within an area or by increasing the areaavailable for the same number of animals. Populations of manywild species have been compressed because of habitatdegradation and loss but, in most cases, there is little or noeffective manner of increasing the amount of available habitat.If unoccupied suitable habitat is available, ‘surplus’ animalscould be removed from one site and translocated to another.This method was used to reduce population density of bighornsheep as a preventive measure to reduce the likelihood ofoutbreaks of pneumonia (86). In most instances, populationdensity is reduced by removing animals. Normally this is doneby killing animals, i.e. by increasing the mortality rate, but apopulation could also be reduced by decreasing reproduction.Control of reproduction has been attempted for pest speciesand there is interest in developing reproductive controlmethods in a few disease situations (29), but there is noinformation available on the actual use of this form ofpopulation reduction for disease management among wildspecies.

Population reduction can be of three general types, namely:focal around a specific site, locally extensive in an area to createa barrier, or generalised over a broad region. All three formshave been used for disease management. The first two are onlyappropriate for diseases that are localised and in which thedistribution is well known or where a very localised effect isdesired. Wobeser reviewed a number of such projects andidentified some general features of population reductionprogrammes (102), as follows:

– Population reduction has usually been aimed at carnivores,and species considered as pests, rather than at game species orspecies considered beneficial by the public. This reflects the


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difficulty in convincing the public of the need for killing‘desirable’ species. This aversion may be reduced if there aremultiple reasons for population reduction. Deblinger et al.described reduction of a deer population on a site extendingover 567 ha that was performed with the aim of preservingvegetation, improving deer condition and reducing risk ofLyme disease in people in the area (26).

– Population reduction has been more effective in preventingentry of disease into an area than in dealing with establisheddisease. For example, there are several instances in whichintensive local depopulation of carnivores in advance of aspreading wave of rabies was successful in preventing spreadinto areas free of the disease. These include depopulation ofvampire bats (Desmodus rotundus) to prevent infection of cattlein Argentina (34), depopulation of foxes in Switzerland (99)and Denmark (64), and depopulation of striped skunks inAlberta along a 30-km strip parallel with the border withSaskatchewan and Montana (40). In these examples, controlwas possible because the disease was moving in a singledirection. Geographical barriers that precluded lateralmovement of the disease aided in some situations.

– Population reduction has been more effective for focaloccurrences than for widely disseminated disease. Radialdepopulation within a 5-km radius was used when raccoonrabies occurred in Ontario, Canada. This was accompanied bytrap-vaccination and release of raccoons within an additional 5- to 10-km zone, and general aerial baiting with vaccine overa larger area (81). It was believed that population reduction wasthe most effective way to deal with animals that might beincubating rabies near the index cases, since vaccination is noteffective in animals in the late stage of the disease. The apparentsuccess of this local action is in contrast to many reports of theapparent failure of general population reduction of carnivoresto deal with enzootic rabies (14, 25, 30, 57, 59).

– Population reduction without habitat modification to makethe area less attractive to the species (or to lower the carryingcapacity) is a temporary measure. The speed with which apopulation recovers depends on the extent of reduction, thesize of the area which influences the amount of recruitmentthrough immigration, and the reproductive rate of the species.Population recovery is highly species- and site-specific. Asexamples, Waltermire found that a population of Richardson’sground squirrels (Spermophilus richardsoni) reduced by 90% inspring for plague control recovered to about 52%-64% of thepre-control level by mid-summer but some degree of reductionpersisted for one year (98). Bögel et al. estimated that Europeanfox populations reduced to 20%-30%, 40%, 60% and 80% ofthe original population would recover to original densitieswithin four, three, two and one year(s), respectively (13).Everard and Everard estimated that poisoning killed 33%-66%of mongooses (Herpestes auropunctatus) in some areas ofGrenada, but that the population recovered in some locationswithin nine months (30).

– There has been a trend away from attempted wide-scaledepopulation to population reduction on a local level.

– Population reduction projects tend to be supported wellwhile disease is highly evident, but lose support and fundingwhen the prevalence of disease decreases. This may allowrecrudescence of disease.

If population reduction is to be used for disease control througheither focal reduction around individual cases or to create abarrier to disease movement, effective surveillance and rapidreporting of cases are necessary, so that control can be appliedin the correct location. This is a serious limitation on thetechnique because intense surveillance usually is not availablefor wild species. It is particularly unreliable for small orinconspicuous species but even for medium-sized and largeanimals the ‘normal’ reporting rate of diseased animals is verypoor. For example, the reporting rate for foxes dying of rabiesin Europe was estimated at 2%-10% (5). The reporting rate islikely to be even lower for unexpected disease occurrences.Hone and Pech estimated that the probability of an individualdiseased feral hog being reported was <0.0015, should foot andmouth disease occur in Australia (48).

The size of the population reduction zone or barrier is critical.If it is too small, infected animals will be missed or will moveacross the barrier; if it is too large, the effort to remove animalsmay be so diluted that insufficient animals will be removed.(For instance, if the radius for population reduction is 2 km, thearea in which population reduction must be performed is about12.5 km2, whereas if the radius is increased to 5 km, the area =78 km2, requiring >6-fold more effort.) The size of the areamust be based on the expected travel distance or home rangeof the species and these will be highly variable in differenthabitat types. Animals infected with some diseases (e.g. rabies),may move considerably greater distances than normal animalsin the same area (82). Muller suggested that a control zone 60-100-km wide was needed for foxes in Denmark (64), Lordused a depopulation zone 15-km wide for rabies control invampire bats (55), and a zone 5-km wide was used for rabiesmanagement in striped skunks (40) and raccoons (81) inCanada.

Reduction of the population density within a restricted areamay have to be accompanied by other actions to prevent theinflux of susceptible animals from the surrounding area becauselocal population reduction ‘may be counter-productive if thesubsequent contact rate is increased because of immigration ofsusceptible animals’ (46). Hone and Bryant proposed atechnique that might be employed to control foot and mouthdisease in feral pigs around a focal outbreak in cattle (47). In themodel, intense depopulation would be conducted in the centralzone at the same time as a pig-proof fence would beconstructed around a perimeter to prevent both immigrationand emigration. Rosatte et al. used a similar zone approach todeal with an incursion of raccoon rabies into Ontario (81).Intense trapping and euthanasia of trapped raccoons and


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striped skunks was performed within 5 km of the initial cases.At the same time, raccoons and skunks were captured in asecond radial zone 5 to 10 km from each case. These animalswere vaccinated, tagged for identification and released. Thiswas supplemented by aerial application of oral vaccine baitsover a broader area surrounding the cases.

It is very important in focal depopulation around isolated casesof disease to be able to apply intense population reductionpressure rapidly. For instance, Pech and Hone suggested, on thebasis of a model, that it would be necessary to eliminate >95%of the feral pigs within an area in less than 21 days to besuccessful in controlling a local outbreak of foot and mouthdisease (69). Rosatte et al. identified the existence of a detailedcontingency plan which could be implemented immediately,and the rapid deployment of staff, as the keys to success of aprogramme to control raccoon rabies in Ontario, Canada (81).

The degree of population reduction required to prevent adisease from spreading or to lead to its extinction is unknownfor most diseases. The value is likely to be highly variable indifferent locations, even for diseases that have a single host. Forinstance, rabies remained enzootic in Ontario at a foxpopulation density which was thought to result in thedisappearance of the disease in Europe (97). The followingexamples are intended only to illustrate the degree ofpopulation reduction that has been suggested as appropriate indifferent circumstances. Waltermire estimated that a groundsquirrel population would have to be reduced by at least 90%for effective management of plague (98). Roberts suggested thatMycobacterium bovis infection could be eliminated from abrushtail possum (Trichosurus vulpecula) population in NewZealand by reducing and maintaining the population at 43% ofits carrying capacity (79). Fornes et al. estimated that theyremoved about 95% of the vampire bats in advance of aspreading wave of rabies (34), and Rosatte et al. estimated that83% to 91% of raccoons were killed in the zone around theinitial cases of raccoon rabies in Ontario (81). ‘Virtualelimination’ and approximately 80% reduction of deerpopulations on two small areas in Massachusetts resulted inreduction in the number of Ixodes dammini ticks in both areasand a reduction in the incidence of Lyme disease in humans onone site (26).

In general, mass population reduction over large areas has onlybeen attempted for the most serious of diseases. Evidence fromearly attempts is difficult to interpret. In many cases, notablythose involving rabies referred to earlier, general populationreduction was considered to have been ineffective. There havebeen suggestions that attempted depopulation of coyotes (Canislatrans) might increase natality and decrease natural mortalityto potentially offset the planned population reduction (22). Insituations in which a disease disappeared from an areafollowing population reduction, there were no detailed studiesto determine the actual contribution by population reduction.Examples of such programmes include massive killing of deer

in California during an outbreak of foot and mouth disease(16), and in Florida as part of a cattle fever tick eradicationprogramme (41) and killing of many foxes in Spain following alocal incursion of rabies (6). An incursion of rabies into theprovince of Alberta led to a massive depopulation of carnivoresbetween 1952 and 1954. The disappearance of the disease wascredited to the population reduction, together with control andvaccination of dogs (7); however, the same epizootic died outin the neighbouring provinces of British Columbia,Saskatchewan and Manitoba without any organisedprogramme of wildlife depopulation (95).

The longest-running programme of non-selective culling of awild population for disease control is the effort to reduce oreliminate Mycobacterium bovis infection in brushtail possums asa source of infection for cattle in New Zealand. The principalmethod used for more than 40 years has been aerialdistribution of baits containing sodium monofluoroacetate(1080) (43). Some general features of this programme areworth noting. There has been no evidence of acquiredphysiological resistance to 1080, although it has been used onup to 2.5 million ha annually; however, a significant proportionof possums survive poisoning operations for a variety of otherreasons (43). Infection among possums is not uniformlydistributed; the highest prevalence occurs in habitats capable ofsupporting the highest density of possums (18). Large- scale,short-term reduction of possum populations seldom has beeneffective because, without follow-up control of possums, theincidence of tuberculosis in cattle regained its previous level (9).Sustained long-term reduction of possum populations to about22% of the pre-control density resulted in a major reduction inthe incidence of tuberculosis in cattle and the prevalence oftuberculosis in possums (17). Caley et al. suggested that if thelevel of possum population reduction was sufficient,tuberculosis could be eradicated from the population (17).

The most severe form of population reduction is totalextirpation of a species from an area. Eradication of a wildspecies has been suggested as a method that might be usedshould a serious animal disease, such as foot and mouth diseasebecome established in a disease-free area, (47, 69) and wasproposed as the method of choice for eliminating brucellosisand tuberculosis from bison in and around Wood BuffaloNational Park in Canada (32). However, the author is aware ofonly two published reports of eradication having been used fordisease control in a free-living species and both were on a verylocal level. Gershman et al. eradicated the surviving eiders, gulls(Larus spp.) and terns (Sterna hirundo) on islands off the coastof Maine following an outbreak of avian cholera among eiders(37). Pursglove et al. used a wetting agent sprayed from aircraftto immobilise over 6,000 American coots (Fulica americana) ina group experiencing avian cholera (74). The birds were thencollected and killed. The efficacy of these actions isquestionable. Eradicaton of the eiders did not preventsubsequent occurrences of the disease among the eiderpopulation in the area (52). Montgomery et al. (63) believed


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that mortality in an outbreak among coots similar to thatdescribed by Pursglove et al. (74) declined because ofpopulation reduction caused by the disease and migration.There are very few reports in which intentional eradication of awild species has been accomplished for any purpose. Theelimination of muskrats (Ondatra zibethicus) from Great Britainby trapping (100) stands as an example that extirpation may bepossible.

The potential for eradicating a population of large animals, suchas might be considered during an incursion of foreign domesticanimal disease, has been tested on two occasions in Australia.Feral pigs on a 50 km2 area were first poisoned with 1,080 baitsand then live pigs were hunted from helicopters. Honeconcluded that ‘eradication would be almost complete, butprobably not entirely so’ using these methods (46). Neither therate of recruitment through immigration from the surroundingcountryside nor the cost to maintain depopulation of the areawere reported. Ridpath and Waithman tested the feasibility oferadicating feral water buffalo (Bubalus bubalis) on a 389 km2

area (78). Using a combination of helicopter round-ups,shooting from helicopters, and shooting from the ground, morethan 97% of the population was removed over a 3.5 monthperiod. These experiments illustrate a fundamental problemwith extirpation. As the population is reduced, the effortrequired for further reduction escalates markedly andelimination of the final few animals may be extremely difficult.It may also be very difficult to determine when and ifextirpation has been accomplished. These experiments wereconducted on small areas (equivalent to circles with a radius of about 4 and 11 km, respectively) on which intensemanagement pressure could be exerted and maintained. Incontrast, Hone and Pech estimated that foot and mouth diseasemight have spread within the feral pig population to cover10,000 km2 to 30,000 km2 prior to the first case beingdiagnosed (48). Based on their experimental trial, Ridpath andWaithman concluded that ‘eradication of buffalo from theirentire range would be an unrealistic objective, botheconomically and practically’ (78).

Total eradication of a population of wild animals that may havebeen exposed to a disease, as has been the case in emergencycontrol operations in domestic animals, is probably impossible,at least in the short-term.

ConclusionManagement of disease in wild animals must be based onsound knowledge of the biology of the disease agent and thespecies affected, and particularly of the population ecology ofthe disease process. The initial step in any management

programme is to clearly define its objective. This might be toprevent introduction of a disease, to reduce the frequency ofoccurrence or effect of a disease, or to eradicate an existingdisease. When the objective has been defined, potentialtechniques for reaching the objective can be considered,together with their advantages and disadvantages. It is alsoimportant to consider in advance the required and availableresources for management. Management may includetechniques to manipulate the disease agent or its vectors, thehost animals, other aspects of the environment, or humanactivities. It is very important that management programmesinclude a continuous monitoring process, so that theeffectiveness of techniques can be measured, and new methodscan be introduced if current methods are ineffective.Programmes should be sufficiently flexible to change withevolving circumstances as the programme proceeds and severalmethods may need to be applied either simultaneously orsequentially during a programme. Public education is avaluable component of many management programmes; bothto gain public support through demonstrating the need formanagement and to change human activities that influence thedisease.

In general, it is easier to prevent the introduction of newdiseases than to control or eradicate existing diseases. Short-term specific measures, such as treating individual animals,disinfection, or dispersing animals from focal areas of infection,are expensive, transient in effect, limited to small areas, andmay have little effect on the general health of the population.Long-term non-specific techniques, such as habitatimprovement, may reduce disease over time as well as havingother beneficial effects. Many of the techniques that have beenused to manage disease in wild animals are of unproveneffectiveness.


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Stratégies de gestion des maladies de la faune sauvageG. Wobeser

RésuméIl existe trois grandes stratégies de gestion des maladies de la faune sauvage : laprévention, la lutte contre les maladies existantes et l’éradication. Les mesuresde gestion peuvent s’appliquer à l’agent pathogène, à la population hôte, àl’habitat de l’hôte ou aux activités humaines. Face aux agents pathogènes, onpeut agir à deux niveaux : la désinfection de l’environnement ou le traitement del’hôte. La désinfection et l’utilisation de pesticides pour détruire les agents ouvecteurs sont limitées à des situations locales ; elles peuvent être nocives pourl’environnement et induire l’acquisition de résistances. Les difficultés liées àl’administration d’un traitement limitent la chimiothérapie à des foyers isolés. Lagestion des populations hôtes peut reposer sur la vaccination, sur la modificationde leur répartition ou de leur densité, ou encore sur leur extirpation de la zone. Lavaccination est la méthode la plus indiquée contre les infections exogènes duesà des microparasites présentant un taux de reproduction peu élevé et chez despopulations qui se renouvellent lentement. La vaccination de masse au moyend’appâts oraux s’est révélée efficace, mais cette stratégie se limite à quelquesgraves maladies. Il est difficile de déplacer les animaux sauvages et lestechniques visant à dissuader les animaux de pénétrer dans une zone deviennentrapidement inefficaces. La mise en place de clôtures n’est possible que danscertaines zones limitées. L’abattage sélectif se limite aux cas dans lesquels lesindividus affectés sont immédiatement identifiables. La réduction d’unepopulation en général s’est révélée peu efficace pour lutter contre les maladies ;en revanche, on a obtenu de bons résultats en diminuant les populations setrouvant à la périphérie d’un foyer ou en créant une zone tampon pour éviter lapropagation d’une maladie. La réduction des populations est une mesuretemporaire. L’éradication d’une population d’animaux sauvages à des fins degestion sanitaire n’a jamais été tentée. En revanche, il est possible de modifierl’habitat pour réduire l’exposition aux agents pathogènes ou pour changer larépartition des hôtes ou leur densité. La gestion des maladies des animauxsauvages implique habituellement une modification des activités humaines. Laprincipale méthode consiste à limiter les mouvements d’animaux sauvages pourprévenir la diffusion des maladies.

Mots-clésÉradication – Faune sauvage – Gestion – Macroparasites – Microparasites – Prévention –Prophylaxie – Transmission – Vecteurs.�

Estrategias de gestión de enfermedades de la fauna salvaje G. Wobeser

ResumenPara gestionar las enfermedades de la fauna salvaje caben tres tipos básicos deestrategia, a saber, prevenir la introducción de la enfermedad, controlar laenfermedad ya presente, o erradicarla. La estrategia de gestión puede centrarseen el agente etiológico, las poblaciones o hábitats del animal huésped o lasactividades humanas. Cuando se opta por atacar el agente patógeno, cabe

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recurrir a la desinfección (para contener su presencia en el medio natural) o altratamiento (para eliminarlo del organismo de los huéspedes). El uso dedesinfectantes y plaguicidas para destruir el agente o sus vectores se limita azonas reducidas, ya que esos productos pueden tener graves efectosambientales o inducir la adquisición de resistencias. La dificultad de administrartratamientos farmacológicos limita también este expediente al ámbito local. Encuanto a las poblaciones del huésped, cabe inmunizarlas, modificar sudistribución o densidad o simplemente extirparlas del lugar. La inmunización esel mejor método para microparásitos exógenos con una tasa de reproducciónbaja y para poblaciones huéspedes que se renuevan lentamente. Aunque se handemostrado fructíferos, los métodos de inmunización masiva con cebos decomida sólo se aplican a unas pocas enfermedades de especial gravedad.Desplazar a los animales salvajes no resulta fácil, y las técnicas paraahuyentarlos de una zona concreta pierden eficacia con rapidez. La colocaciónde vallas sólo es factible en áreas reducidas. El sacrificio selectivo se reserva alos casos en que resulta sencillo detectar a los individuos afectados. Aunque lareducción general de poblaciones no ha sido muy útil en la lucha contraenfermedades, la reducción alrededor de un foco infeccioso o la creación debarreras al movimiento de la enfermedad, en cambio, sí han dado buenosresultados. La reducción de una población es en cualquier caso una medidatemporal. Nunca se ha intentado erradicar una población de animales salvajescomo medida de gestión sanitaria. La modificación del hábitat es un posibleexpediente para reducir la exposición a agentes patógenos o alterar ladistribución o densidad de las poblaciones huéspedes. Por regla general, lagestión de enfermedades de la fauna salvaje requiere introducir cambios en lasactividades humanas. El método más importante es el de restringir el traslado deanimales salvajes para evitar que una enfermedad se desplace.

Palabras claveControl – Erradicación – Fauna salvaje – Gestión – Macroparásitos – Microparásitos –Prevención – Transmisión – Vectores.�

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